Taxonomic diversity of ant (Hymenoptera: Formicidae) assemblages in forest remnants in the Northeast of Argentina

Dario D. Larrea; Helga C. Achitte-Schmutzler; José M. Sánchez

doi:10.25260/EA.23.33.1.0.2082

Authors

Dario D. Larrea Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Universidad Nacional del Nordeste, Facultad de Ciencias Exactas y Naturales y Agrimensura, Biología de los Artrópodos. Corrientes, Argentina https://orcid.org/0000-0002-8808-1049
Helga C. Achitte-Schmutzler CONICET. Universidad Nacional del Nordeste, Facultad de Ciencias Exactas y Naturales y Agrimensura, Biología de los Artrópodos. Corrientes, Argentina
José M. Sánchez CONICET, Instituto de Diversidad y Ecología Animal (IDEA). Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Centro de Zoología Aplicada. Córdoba, Argentina

DOI:

https://doi.org/10.25260/EA.23.33.1.0.2082

Keywords:

taxonomic diversity, forest, Argentina, ants

Abstract

Argentina is among the ten countries in the world with loss of large areas of forests in recent years. Deforestation leads to an inevitable loss of biodiversity and the fragmentation of natural environments, with increased extinctions of species in small patches. Ants are present in all terrestrial ecosystems and play key ecological roles. This study aimed to analyse how ant assemblages vary in different forest remnants of the Northeast Argentina (NEA) from the approach of taxonomic diversity, which involve the linnean classifications relationships of the taxa. The ants were collected by hand collecting and pitfall trapping techniques in theforests of 15 NEA localities during the warm months in 2015-2018. In total, 600 samples, 10741 individuals and 94 ant species were obtained. In this way, 94 species distributed in 41 genera, 14 tribes and 9 subfamilies were obtained. Myrmicinae, Fomicinae and Ponerinae presented the highest specific richness. The results of taxonomic distinctness (Δ+) and average taxonomic variation (Λ+) demonstrated that all localities fell within the expected average for estimated models. The beta diversity, measured by the species dissimilarity (1-βJ) and taxonomic dissimilarity (1-∆T), reflected in the NMDS and cluster analyses, proved that the localities in the Iberá Reserve (Corrientes), differ from the rest both in the specific composition and in the phylogenetic relationships between them. This could indicate a typical ant microfauna of the Iberá Reserve.

References

Agosti, D., J. D. Majer, L. Alonso, and T. R. Schultz. 2000. Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington DC, United States.

De Angelo, C., A. Paviolo, and M. Di Bitetti. 2011. Differential impact of landscape transformation on pumas (Puma concolor) and jaguars (Panthera onca) in the Upper Paraná Atlantic Forest. Diversity and Distributions 17:422-436. https://doi.org/10.1111/j.1472-4642.2011.00746.x.

Anu, A., and T. K. Sabu. 2007. Biodiversity analysis of forest litter ant assemblages in the wayanad region of western ghats using taxonomic and conventional diversity measures. Journal of Insect Science 7:1-13. https://doi.org/10.1673/031.007.0601.

APN. 2017. Plan de Gestión. Page Parque Nacional Iberá.

Arana, M. D., G. A. Martínez, A. J. Oggero, E. S. Natale, and J. J. Morrone. 2017. Map and shapefile of the biogeographic provinces of Argentina. Zootaxa 4341:420-422. https://doi.org/10.11646/zootaxa.4341.3.6.

Arana, M. D., E. Natale, N. Ferretti, G. Romano, A. Oggero, G. Martínez, P. Posadas, and J. J. Morrone. 2021. Esquema Biogeográfico de la República Argentina. Page (T. Opera lilloana 56, Fundación Miguel Lillo, Ed.). Tucumán, Argentina. Pp. 240.

Arbino, M. O., and M. C. Godoy. 2001. Relaciones biológicas entre hormigas (Insecta: Hymenoptera, Formicidae) y termites (Insecta: Isoptera) en el macrosistema Iberá.

Bacaro, G., E. Baragattia, and A. Chiarucci. 2009. Using taxonomic data to assess and monitor biodiversity: are the tribes still fighting? Journal of Environmental Monitoring 11:798-801. https://doi.org/10.1039/b818171n.

Bacaro, G., C. Ricotta, and S. Mazzoleni. 2007. Measuring beta-diversity from taxonomic similarity. Journal of Vegetation Science 18:793-798. https://doi.org/10.1111/j.1654-1103.2007.tb02595.x.

Bacaro, G., D. Rocchini, C. Duprè, M. Diekmann, F. Carnesecchi, V. Gori, and A. Chiarucci. 2012. Absence of distance decay in the similarity of plots at small extent in an urban brownfield. Community Ecology 13:36-44. https://doi.org/10.1556/ComEc.13.2012.1.5.

Barbosa, O., and P. A. Marquet. 2002. Effects of forest fragmentation on the beetle assemblage at the relict forest of Fray Jorge, Chile. Oecologia 132:296-306. https://doi.org/10.1007/s00442-002-0951-3.

Bestelmeyer, B. T., and J. A. Wiens. 1996. The Effects of Land Use on the Structure of Ground-Foraging Ant Communities in the Argentine Chaco. Ecological Applications 6:1225-1240. https://doi.org/10.2307/2269603.

Bishop, T. R., M. P. Robertson, B. J. van Rensburg, and C. L. Parr. 2015. Contrasting species and functional beta diversity in montane ant assemblages. Journal of Biogeography 42:1776-1786. https://doi.org/10.1111/jbi.12537.

Bolton, B. 2022. AntCat - An online catalog of the ants of the world. URL: antcat.org.

Brooks, T. M., R. A. Mittermeier, G. A. B. Da Fonseca, J. Gerlach, M. Hoffmann, J. F. Lamoreux, C. G. Mittermeier, J. D. Pilgrim, and A. S. L. Rodrigues. 2006. Global biodiversity conservation priorities. Science 313:58-61. https://doi.org/10.1126/science.1127609.

Cabrera, A., and A. Willink. 1980. Biogeografıa de America Latina. 2a edicion corregida. Monografıa 13. Serie de Biologıa. Secretarıa General de la Organizacion de los Estados Americanos., Washington DC, Estados Unidos.

Calcaterra, L. A., L. Chifflet, F. Cuezzo, and A. F. Sánchez-Restrepo. 2021. Diversity of ground-dwelling ants across three severely threatened South American subtropical forests: are diversity patterns influenced by spatial or climatic variables? Insect Conservation and Diversity 15:86-101. https://doi.org/10.1111/icad.12537.

Calcaterra, L. A., F. Cuezzo, S. M. Cabrera, and J. A. Briano. 2010. Ground Ant Diversity (Hymenoptera: Formicidae) in the Iberá Nature Reserve, the Largest Wetland of Argentina. Annals of the Entomological Society of America 103:71-83. https://doi.org/10.1603/008.103.0110.

Calderón-Patrón, J. M., C. E. Moreno, and I. Zuria. 2012. La diversidad beta: medio siglo de avances. Revista Mexicana de Biodiversidad 83:83:879-891. https://doi.org/10.22201/ib.20078706e.2012.3.992.

Carnevali, R. 1994. Fitogografía de la Provincia de Corrientes. Gobierno de la Provincia de Corrientes. Instituto nacional de Tecnología Agropecuaria, Corrientes, Argentina.

Castro, F. S. de, P. G. Da Silva, R. Solar, G. W. Fernandes, and F. de S. Neves. 2020. Environmental drivers of taxonomic and functional diversity of ant communities in a tropical mountain. Insect Conservation and Diversity 13:393-403. https://doi.org/10.1111/icad.12415.

Chao, A., C. H. Chiu, and L. Jost. 2010. Phylogenetic diversity measures based on Hill numbers. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3599-3609. https://doi.org/10.1098/rstb.2010.0272.

Clarke, K. R., and R. N. Gorley. 2001. PRIMERv5: user manual/tutorial. PRIMER-E. Plymouth, United Kingdom.

Clarke, K. R., and R. M. Warwick. 1998. A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35:523-531. https://doi.org/10.1046/j.1365-2664.1998.3540523.x.

Clarke, K. R., and R. M. Warwick. 2001. A further biodiversity index applicable to species lists : variation in taxonomic distinctness. Marine Ecology Progress Series 216:265-278. https://doi.org/10.3354/meps216265.

Correa Ayram, C. A., M. E. Mendoza, A. Etter, and D. R. Pérez Salicrup. 2017. Anthropogenic impact on habitat connectivity: A multidimensional human footprint index evaluated in a highly biodiverse landscape of Mexico. Ecological Indicators 72:895-909. https://doi.org/10.1016/j.ecolind.2016.09.007.

Cuezzo, F., and D. D. Larrea. 2022. Formicidae (Hymenoptera) species from Argentina and Uruguay. URL: biodar.unlp.edu.ar/formicidae/index.html.

Devictor, V., D. Mouillot, C. Meynard, F. Jiguet, W. Thuiller, and N. Mouquet. 2010. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: The need for integrative conservation strategies in a changing world. Ecology Letters 13:1030-1040. https://doi.org/10.1111/j.1461-0248.2010.01493.x.

Dinerstein, E., D. M. Olson, D. J. Graham, A. L. Webster, S. A. Primm, M. P. Bookbinder, and G. Ledec. 1995. A conservation assessment of the terrestrial ecoregions of Latin America and the Caribbean. The World Bank, Washington, DC, EEUU. https://doi.org/10.1596/0-8213-3295-3.

Dubois, A. 2003. The relationships between taxonomy and conservation biology in the century of extinctions. Comptes Rendus - Biologies 326:9-21. https://doi.org/10.1016/S1631-0691(03)00022-2.

FAO. 2016. Global Forest Resources Assessment 2015 How are the world’s forests changing? Food and agriculture organization of the United Nations. Rome.

Fernández, F., and S. Sendoya. 2004. Special issue: List of Neotropical Ants. Número monográfico: Lista de las hormigas neotropicales. Biota Colombiana 5(1):3-93.

Fisher, B. L. 1999. Ant diversity patterns along an elevational gradient in the Réserve Naturelle Intégrale d’Andohahela. Fieldiana: Zoology 94:129-147.

Forest, F., R. Grenyer, M. Rouget, T. J. Davies, R. M. Cowling, D. P. Faith, A. Balmford, J. C. Manning, Ş. Procheş, M. Van Der Bank, G. Reeves, T. A. J. Hedderson, and V. Savolainen. 2007. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445:757-760. https://doi.org/10.1038/nature05587.

García de Jesús, S., C. E. Moreno, M. Á. Morón, I. Castellanos, and N. P. Pavón. 2016. Integrando la estructura taxonómica en el análisis de la diversidad alfa y beta de los escarabajos Melolonthidae en la Faja Volcánica Transmexicana. Revista Mexicana de Biodiversidad 87:1033-1044. https://doi.org/10.1016/j.rmb.2016.06.003.

Ginzburg, R., and J. Adamoli. 2006. Situación ambiental en el Chaco Húmedo. Pp. 180-195 in A. Brown, U. Martinez Ortiz, M. Acerbi and J. Corchera (eds.). La situación ambiental Argentina 2005.

Gómez Lutz, M. C., and M. C. Godoy. 2010. Diversidad y grupos funcionales de Formicidae (Insecta , Hymenoptera) de la reserva natural educativa Colonia Benítez (Provincia del Chaco, Argentina). Revista FABICIB 14:180-195. https://doi.org/10.14409/fabicib.v14i1.863.

Granados-Sánchez, D., G. López, and J. Gama. 1999. Fragmentación del hábitat y manejo de áreas protegidas. Revista Chapingo, serie Ciencias Forestales y del Ambiente 5:5-13.

Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1):1-9.

Hanisch, P. E., L. A. Calcaterra, M. Leponce, R. Achury, A. V Suarez, R. R. Silva, and C. Paris. 2015. Check list of ground-dwelling ant diversity (Hymenoptera: Formicidae) of the Iguazú National Park with a comparison at regional scale. Sociobiology 62:213-227. https://doi.org/10.13102/sociobiology.v62i2.213-227.

Hanisch, P. E., P. D. Lavinia, A. V. Suárez, D. A. Lijtmaer, M. Leponce, C. I. Paris, and P. L. Tubaro. 2017. Mind the gap! Integrating taxonomic approaches to assess ant diversity at the southern extreme of the Atlantic Forest. Ecology and Evolution 7:10451-10466.

Hanisch, P. E., A. V Suárez, P. L. Tubaro, and C. I. Paris. 2018. Co-occurrence Patterns in a Subtropical Ant Community Revealed by Complementary Sampling Methodologies. Environmental Entomology 47:1402-1412. https://doi.org/10.1093/ee/nvy143.

Hölldobler, B., and E. O. Wilson. 1990. The Ants. Harvard University Press. Cambridge, Massachusetts, United States. Pp. 746.

Hoyos, L. E., A. M. Cingolani, M. Zak, M. V. Vaieretti, D. E. Gorla, and M. Cabido. 2012. Deforestation and precipitation patterns in the arid Chaco forests of central Argentina. Applied Vegetation Science 16:260-271. https://doi.org/10.1111/j.1654-109X.2012.01218.x.

Hubbell, S. P. 2011. The unified neutral theory of biodiversity and biogeography. Princeton University Press. https://doi.org/10.1515/9781400837526.

Izsak, C., and A. R. G. Price. 2001. Measuring β-diversity using a taxonomic similarity index, and its relation to spatial scale. Marine Ecology Progress Series 215:69-77. https://doi.org/10.3354/meps215069.

Kaspari, M., and J. Majer. 2000. Using ants to monitor environmental change. Page Ants: Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington DC, United States.

Laliberte, E., P. Legendre, S. Ecology, and N. January. 2014. A distance-based framework for measuring functional diversity from multiple traits. A distance-based framework for measuring from multiple traits functional diversity Ecology 91(1):299-305. https://doi.org/10.1890/08-2244.1.

Larrea, D. D., G. Avalos, and I. Zanone. 2022a. Diversity and functional groups of ants in Citrus sinensis crop field with different watering regime. Boletín de la Sociedad Zoológica del Uruguay 31:e31.1.2.

Larrea, D. D., M. I. Dufek, and M. P. Damborsky. 2022b. Terrestrial Ant Assemblages (Hymenoptera: Formicidae) in Protected Forests and Grasslands in Three Ecoregions of Corrientes Province, Argentina. Environmental Entomology 51:360-369. https://doi.org/10.1093/ee/nvac008.

Leonard, D. R. P., K. R. Clarke, P. J. Somerfield, and R. M. Warwick. 2006. The application of an indicator based on taxonomic distinctness for UK marine biodiversity assessments 78:52-62. https://doi.org/10.1016/j.jenvman.2005.04.008.

Leponce, M., L. Theunis, J. H. C. Delabie, and Y. Roisin. 2004. Scale dependence of diversity measures in a leaf-litter ant assemblage. Ecography 27:253-267. https://doi.org/10.1111/j.0906-7590.2004.03715.x.

Losos, J. B. 1994. Historical contingency and lizard community ecology. Pp. 319-333 in L. J. Vitt and E. R. Pianka (eds.). Lizard Ecology: Historical and Experimental Perspectives. Princeton University Press, New Jersey. https://doi.org/10.1515/9781400863945.319.

Majer, J. D., G. Orabi, and L. Bisevac. 2007. Ants (Hymenoptera: Formicidae) pass the bioindicator scorecard. Myrmecological News 10:69-76.

Moreno, C. E., G. Castillo-Campos, and J. R. Verdú. 2009. Taxonomic Diversity as Complementary Information to Assess Plant Species Diversity in Secondary Vegetation and Primary Tropical Deciduous Forest. Journal of Vegetation Science 20:935-943. https://doi.org/10.1111/j.1654-1103.2009.01094.x.

Morrone, J. J. 2000. What is the Chacoan subregion? Neotropica 46:51-68.

Morrone, J. J. 2006. Biogeographic Areas and Transition Zones of Latin America and the Caribbean Islands Based on Panbiogeographic and Cladistic Analyses of the Entomofauna. Annual Review of Entomology 51:467-494. https://doi.org/10.1146/annurev.ento.50.071803.130447.

Nekola, J. C., and J. H. Brown. 2007. The wealth of species : ecological communities , complex systems and the legacy of Frank Preston. Ecology Letters 10(3):188-196. https://doi.org/10.1111/j.1461-0248.2006.01003.x.

Nekola, J. C., and P. S. White. 1999. The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26:867-878. https://doi.org/10.1046/j.1365-2699.1999.00305.x.

Orfeo, O. 2005. Historia geológica del Iberá, provincia de Corrientes, como escenario de biodiversidad. INSUGEO, Miscelánea 14:71-78.

Pavlacky, D. C., H. P. Possingham, A. J. Lowe, P. J. Prentis, D. J. Green, and A. W. Goldizen. 2012. Anthropogenic landscape change promotes asymmetric dispersal and limits regional patch occupancy in a spatially structured bird population. Journal of Animal Ecology 81:940-952. https://doi.org/10.1111/j.1365-2656.2012.01975.x.

Pereira Gomes, J., L. I. Bet Stedille, J. E. de Freitas Milani, K. Montibeller-Silva, A. Mantovani, and R. Lopes da Costa Bortoluzzi. 2020. Beta diversity as an indicator of priority areas for Myrtaceae assemblage conservation in Subtropical Araucaria Forest. Biodiversity and Conservation 29:1361-1379. https://doi.org/10.1007/s10531-020-01940-8.

Pérez-Sánchez, A. J., W. P. Mackay, and F. Otálora-Luna. 2018. Historia Natural de Camponotus simillimus indianus Forel, 1879 (Hymenoptera: Formicidae): una hormiga domiciliaria en los andes venezolanos. Saber 30:539-556.

Philpott, S. M., I. Perfecto, I. Armbrecht, and C. L. Parr. 2010. Ant diversity and function in disturbed and changing habitats. Pp. 137-156 in L. Lach, C. L. Parr and K. L. Abbott (eds.). Ant Ecology. Oxford University Press, Oxford, England, United Kingdom. https://doi.org/10.1093/acprof:oso/9780199544639.003.0008.

Pianka, E. R. 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4:53-74. https://doi.org/10.1146/annurev.es.04.110173.000413.

Qian, H., N. G. Swenson, and J. Zhang. 2013. Phylogenetic beta diversity of angiosperms in North America. Global Ecology and Biogeography 22:1152-1161. https://doi.org/10.1111/geb.12076.

Ricotta, C., G. Bacaro, M. Marignani, S. Godefroid, and S. Mazzoleni. 2012. Computing diversity from dated phylogenies and taxonomic hierarchies: Does it make a difference to the conclusions? Oecologia 170:501-506. https://doi.org/10.1007/s00442-012-2318-8.

Sanderson, E. W., M. Jaiteh, M. A. Levy, K. H. Redford, A. V. Wannebo, and G. Woolmer. 2002. The human footprint and the last of the wild. BioScience 52:891-904. https://doi.org/10.1641/0006-3568(2002)052[0891:THFATL]2.0.CO;2.

Santoandré, S., J. Filloy, G. A. Zurita, and M. I. Bellocq. 2019. Ant taxonomic and functional diversity show differential response to plantation age in two contrasting biomes. Forest Ecology and Management 437:304-313. https://doi.org/10.1016/j.foreco.2019.01.021.

Schweiger, O., S. Klotz, W. Durka, and I. Kühn. 2008. A comparative test of phylogenetic diversity indices. Oecologia 157:485-495. https://doi.org/10.1007/s00442-008-1082-2.

Silvestre, R., C. Roberto, F. Brandão, and R. Rosa. 2003. Grupos funcionales de hormigas : El caso de los gremios del Cerrado. Pp. 113-148 in F. Fernández (ed.). Introducción a las hormigas de la región neotropical. Bogota, Colombia.

Srivastava, D. S., M. W. Cadotte, A. A. M. Macdonald, R. G. Marushia, and N. Mirotchnick. 2012. Phylogenetic diversity and the functioning of ecosystems. Ecology Letters 15:637-648. https://doi.org/10.1111/j.1461-0248.2012.01795.x.

Stratford, J. A., and P. C. Stouffer. 2015. Forest fragmentation alters microhabitat availability for Neotropical terrestrial insectivorous birds. Biological Conservation 188:109-115. https://doi.org/10.1016/j.biocon.2015.01.017.

Terlizzi, A., M. J. Anderson, S. Bevilacqua, S. Fraschetti, M. Włodarska-Kowalczuk, and K. E. Ellingsen. 2009. Beta diversity and taxonomicsufficiency: Do higher-level taxa reflect heterogeneity in species composi-tion? Diversity and Distributions 15:450-458. https://doi.org/10.1111/j.1472-4642.2008.00551.x.

Theunis, L. 2005. Leaf litter ant assemblage in a natural fragmented dry forest in the argentinian chaco promoteurs.

Vasconcelos, H. L., J. M. S. Vilhena, K. G. Facure, and A. L. K. M. Albernaz. 2010. Patterns of ant species diversity and turnover across 2000 km of Amazonian floodplain forest. Journal of Biogeography 37:432-440. https://doi.org/10.1111/j.1365-2699.2009.02230.x.

Villéger, S., P. M. Novack-Gottshall, and D. Mouillot. 2011. The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time. Ecology Letters 14:561-568. https://doi.org/10.1111/j.1461-0248.2011.01618.x.

Volante, J. N., and L. Seghezzo. 2018. Can’t see the forest for the trees: Can declining deforestation trends in the argentinian chaco region be ascribed to efficient law enforcement? Ecological Economics 146:408-413. https://doi.org/10.1016/j.ecolecon.2017.12.007.

Webb, C. O., D. D. Ackerly, M. A. McPeeK, and M. J. Donoghue. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33:475-505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448.

Wiens, J. A. 1977. On Competition and Variable Environments: Populations may experience “ecological crunches” in variable climates, nullifying the assumptions of competition theory and limiting the usefulness of short-term studies of population patterns. American Scientist 65:590-597.

Wilson, E. O. 2003. Pheidole in the New World: A Dominant, Hyperdiverse Ant Genus. Harvard University Press, Cambridge, Massachusetts, United States.

Winter, M., V. Devictor, and O. Schweiger. 2013. Phylogenetic diversity and nature conservation: Where are we? Trends in Ecology and Evolution 28:199-204. https://doi.org/10.1016/j.tree.2012.10.015.

Zak, M. R., M. Cabido, D. Caceres, and S. Díaz. 2008. What Drives Accelerated Land Cover Change in Central Argentina? Synergistic Consequences of Climatic, Socioeconomic, and Technological Factors. Environmental Management 42:181-189. https://doi.org/10.1007/s00267-008-9101-y.